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Rare Morph Lake Malawi Mbuna Cichlids Benefit from Reduced Aggression from Con- and Hetero-Specifics

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Rare Morph Lake Malawi Mbuna Cichlids Benefit from Reduced Aggression from Con- and Hetero-Specifics bioRxiv preprint doi: https://doi.org/10.1101/2021.04.08.439056; this version posted April 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 1 Rare morph Lake Malawi mbuna cichlids benefit from reduced aggression from con- and hetero-specifics 2 Running title: Reduced aggression benefits rare morph mbuna 3 4 Alexandra M. Tyers*, Gavan M. Cooke & George F. Turner 5 School of Biological Sciences, Bangor University, Deniol Road, Bangor. Gwynedd. Wales. UK. LL57 2UW 6 * Current address: Max Planck Institute for Biology of Ageing, Joseph-Stelzmann-Straße 9B, 50931, Köln 7 8 Corresponding author: A.M. Tyers, [email protected] 9 10 Abstract 11 Balancing selection is important for the maintenance of polymorphism as it can prevent either fixation of one 12 morph through directional selection or genetic drift, or speciation by disruptive selection. Polychromatism can 13 be maintained if the fitness of alternative morphs depends on the relative frequency in a population. In 14 aggressive species, negative frequency-dependent antagonism can prevent an increase in the frequency of rare 15 morphs as they would only benefit from increased fitness while they are rare. Heterospecific aggression is 16 common in nature and has the potential to contribute to rare morph advantage. Here we carry out field 17 observations and laboratory aggression experiments with mbuna cichlids from Lake Malawi, to investigate the 18 role of con- and heterospecific aggression in the maintenance of polychromatism and identify benefits to rare 19 mores which are likely to result from reduced aggression. Within species we found that males and females bias 20 aggression towards their own morph, adding to the evidence that inherent own-morph aggression biases can 21 contribute to balancing selection. Over-representation of rare morph territory owners may be influenced by 22 two factors; higher tolerance of different morph individuals as neighbours, and ability of rare morphs to spend 23 more time feeding. Reduced aggression to rare morph individuals by heterospecifics may also contribute to rare 24 morph advantage. 25 26 Key words: Malawi, cichlid, blotch polymorphism, aggression, rare morph advantage 27 28 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.08.439056; this version posted April 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 29 Introduction 30 Permanent polymorphism, the presence of multiple genetically determined morphological or behavioural 31 phenotypes within a population, is common in nature and indicates some type of selective balance between 32 morphs. Balancing selection is important for the maintenance of polymorphism as it can prevent either fixation 33 of one morph through directional selection or genetic drift, or speciation by disruptive selection (Huxley 1955; 34 Wellenreuther et al. 2014; Kim et al. 2019). Polychromatism (colour polymorphism) can be maintained if the 35 fitness of alternative morphs differs in time or space in heterogeneous environments, or if the fitness of a 36 phenotype depends on its relative frequency in a population (Hughes et al. 2013; Pérez i de Lanuza et al. 2017; 37 Surmacki et al. 2013; Svensson 2017; Henze et al. 2018). 38 In many taxa, species-recognition cues have diverged through reproductive or antagonistic character 39 displacement to reduce hybridisation or unnecessary exertion and risk of injury among heterospecifics which 40 are not in direct competition for mates or resources (Seehausen & Schluter 2004; Grether et al. 2009). Rare 41 colour morphs can benefit from lack of recognition by receiving less mating-related harassment (Takahashi et al. 42 2010) or less intrasexual aggression from conspecifics (Dijkstra et al. 2008; Lehtonen 2014; Pérez i de Lanuza G 43 et al. 2017; Scali et al. 2020). In aggressive species, negative frequency-dependent antagonism, generated 44 through either evolution of an own-morph bias (Dijkstra et al. 2008; Lehtonen 2014; Scali et al. 2020) or by a 45 dynamic common morph bias based on experience (Bolnick et al. 2016), can prevent an increase in the 46 frequency of rare morphs as they would only benefit from increased fitness (due to reduced aggression) while 47 they are rare (Seehausen & Schluter 2004; Dijstra et al. 2007; Bolnick et al. 2016). 48 The existence of conspecific aggression biases does not preclude heterospecific aggression completely. 49 Indeed, resent studies suggest that heterospecific aggression as a result of resource competition and 50 reproductive interference may be more common than previously assumed (Grether et al. 2009; Drury et al. 51 2020). Regardless of whether heterospecific aggression is due to convergence in territorial signals among 52 species competing for resources or due to misdirection of aggression because closely related species still share 53 similar signals (Losin et al. 2016), in a variety of taxa aggression is often higher among more similar coloured 54 than more differently coloured species (Genner et al. 1999; Pauers et al. 2008; Anderson & Grether 2010; Losin 55 et al. 2016). In taxa where multiple ecologically and phenotypically similar species co-exist in the same habitat 56 there is therefore potential for rare morphs to benefit not only from reduced conspecific aggression, but also 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.08.439056; this version posted April 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 57 from reduced heterospecific aggression. A recent study of Midas cichlids, however, demonstrated increased 58 aggression towards rare heterospecific morphs and suggested that this disadvantage may help to explain their 59 lower frequency in natural populations (Lehtonen et al. 2015). The role of heterospecific aggression in relation 60 to polychromatism requires further exploration to improve our understanding of how this may contribute to its 61 evolution and maintenance. 62 The mbuna cichlids of Lake Malawi (and the closely-related ecologically-similar Mbipi of Lake Victoria) 63 provide an excellent system for the investigation of colour polymorphism . Mbuna inhabit densely packed multi- 64 species communities in the shallow-waters and identify conspecific mates and rivals predominantly by their 65 species-specific colour and pattern (e.g. Seehausen & van Alphen 1998; Couldridge & Alexander 2002; Jordan 66 2008; Pauers et al. 2008). Several species display a polychromatism characterised by the presence of rare 67 “blotched” morph individuals, which occur at different frequencies in different species and populations (Lande 68 et al. 2001; Ribbink et al. 1983; Konings 2007). While it is likely that predation has played some role in the 69 evolution of this polychromatism (Seehausen et al. 1999; Streelman et al. 2003; Maan et al. 2008), and mate 70 choice may have been involved in the evolution of (partial) sex-linkage (Seehausen et al. 1999; Lande et al. 71 2001; Roberts et al. 2009), it is thought that intrasexual competition plays a large role in its maintenance 72 (Dijkstra et al. 2008; Dijkstra et al. 2009b). Although in most species the frequency of rare morphs remains 73 relatively low in all populations, in some, for example Maylandia callainos at Thumbi West Island in Lake 74 Malawi, rare morphs can occur with higher frequency, which allows greater ease of observation and collection. 75 Here we used this population to conduct field observations and laboratory behavioural experiments to test 76 alternative hypotheses regarding aggression biases: Do both morphs preferentially direct aggression towards 77 the common (presumably ancestral) morph, or is there an own-morph bias? An own-morph bias could be 78 sufficient to maintain polymorphism through negative frequency-dependent selection, while a common-morph 79 bias would suggest that an additional frequency-dependent process would be necessary to limit an increase in 80 the number of rare morph individuals. We also test for aggression biases towards the common and rare morph 81 from a closely related heterospecific to assess whether this may contribute to balancing selection. We aim to 82 identify potential benefits to rare morphs, which may occur as a result of receiving less aggression, in the 83 natural environment. Additionally, as differences in selection pressures on each sex, due to differences in the 84 type of competition they experience (competition for mates among males and competition for non-mating 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.08.439056; this version posted April 9, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. 85 resources among females) can result in sex differences in the types of aggressive behaviour used during 86 contests (Arnott & Elwood 2009), we also test for sex-differences in aggressive behaviour and aggression biases. 87 88 Methods 89 90 Study system 91 Maylandia callainos (= Pseudotropheus callainos or Metriaclima callainos) is a member of the ‘mbuna’ complex 92 of rocky shore cichlid fishes endemic to Lake Malawi. Populations of M. callainos are found in shallow water, 93 with peak population density between 3 – 10m (full range 0 – 25m). Their natural range is confined to the 94 northern end of Lake Malawi, where they are often found in sympatry with the more widely distributed 95 ecologically similar congeneric M.
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